Counteraction of antibiotic production and degradation stabilizes microbial communities

Mathematical modelling and simulations reveal that including antibiotic degraders in ecological models of microbial species interaction allows the system to robustly move towards an intermixed stable state, more representative of real-world observations. Microbial community structure Understanding h...

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Veröffentlicht in:Nature (London) 2015-05, Vol.521 (7553), p.516-519
Hauptverfasser: Kelsic, Eric D., Zhao, Jeffrey, Vetsigian, Kalin, Kishony, Roy
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Sprache:eng
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Zusammenfassung:Mathematical modelling and simulations reveal that including antibiotic degraders in ecological models of microbial species interaction allows the system to robustly move towards an intermixed stable state, more representative of real-world observations. Microbial community structure Understanding how stability in multispecies communities is maintained in the face of negative interactions via antibiotic production is a key goal in microbial ecology. Most ecological models for antibiotic interactions assume pairwise relationships between species that result in rock–scissor–paper type cycling and spatial separation. This doesn't reflect the in situ observations though, where communities are far more intermixed. Instead, Eric Kelsic and colleagues propose a three-species interaction assay, in which one species is capable of antibiotic degradation. Using a mixture of modelling and experimental validation, the authors show that including antibiotic degraders allows the system to robustly move towards an intermixed stable state. A major challenge in theoretical ecology is understanding how natural microbial communities support species diversity 1 , 2 , 3 , 4 , 5 , 6 , 7 , 8 , and in particular how antibiotic-producing, -sensitive and -resistant species coexist 9 , 10 , 11 , 12 , 13 , 14 , 15 . While cyclic ‘rock–paper–scissors’ interactions can stabilize communities in spatial environments 9 , 10 , 11 , coexistence in unstructured environments remains unexplained 12 , 16 . Here, using simulations and analytical models, we show that the opposing actions of antibiotic production and degradation enable coexistence even in well-mixed environments. Coexistence depends on three-way interactions in which an antibiotic-degrading species attenuates the inhibitory interactions between two other species. These interactions enable coexistence that is robust to substantial differences in inherent species growth rates and to invasion by ‘cheating’ species that cease to produce or degrade antibiotics. At least two antibiotics are required for stability, with greater numbers of antibiotics enabling more complex communities and diverse dynamic behaviours ranging from stable fixed points to limit cycles and chaos. Together, these results show how multi-species antibiotic interactions can generate ecological stability in both spatially structured and mixed microbial communities, suggesting strategies for engineering synthetic ecosystems and highlighting the importance of toxin pro
ISSN:0028-0836
1476-4687
DOI:10.1038/nature14485